Induction of Systemic Resistance in Cucumber by Hypovirulent Binucleate Rhizoctonia against Anthracnose Caused by Colletotrichum orbiculare
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Tropical Life Sciences Research, 30(1), 109–122, 2019
Induction of Systemic Resistance in Cucumber by Hypovirulent Binucleate
Rhizoctonia against Anthracnose Caused by Colletotrichum orbiculare
1
A. Muslim*, 2Mitsuro Hyakumachi, 3Koji Kageyama and 1Suwandi Suwandi
1
Department of Plant Protection, Faculty of Agriculture, Sriwijaya University, Jl. Raya
Palembang-Prabumulih, Km. 32, Inderalaya, Ogan Ilir 30662, Indonesia
2
Laboratory of Plant Disease Science, Faculty of Agriculture, Gifu University, Yanagido
1-1,501-1193 Gifu, Japan
3
River Basin Research Center, Gifu University, Gifu 501-1193, Japan
Published date: 31 January 2019
To cite this article: A. Muslim, Mitsuro Hyakumachi, Koji Kageyama and Suwandi
Suwandi. (2019). Induction of systemic resistance in cucumber by hypovirulent binucleate
Rhizoctonia against anthracnose caused by Colletotrichum orbiculare. Tropical Life
Sciences Research 30(1): 109–122. https://doi.org/10.21315/tlsr2019.30.1.7
To link to this article: https://doi.org/10.21315/tlsr2019.30.1.7
Abstract: Treatment with hypovirulent binucleate Rhizoctonia (HBNR) isolates induced
systemic resistance against anthracnose infected by Colletotrichum orbiculare in cucumber,
as there were no direct interaction between HBNR and C. orbiculare. This is because of the
different distances between HBNR and C. orbiculare, where the root was treated with HBNR
isolate and C. orbiculare was challenged and inoculated in leaves or first true leaves were
treated with HBNR isolate and C. orbiculare was challenged and inoculated in second true
leaves. The use of barley grain inocula and culture filtrates of HBNR significantly reduced
the lesion diameter compared to the control (p = 0.05). The total lesion diameter reduction
by applying barley grain inoculum of HBNR L2, W1, W7, and Rhv7 was 28%, 44%, 39%,
and 40%, respectively. Similar results was also observed in treatment using culture filtrate,
and the reduction of total lesion diameter by culture filtrate of HBNR L2, W1, W7, and Rhv7
was 45%, 46%, 42%, and 48%, respectively. When cucumber root was treated with culture
filtrates of HBNR, the lignin was enhanced at the pathogen penetration, which is spread
along the epidermis tissue of cucumber hypocotyls. Peroxidase activity in hypocotyls in
the treated cucumber plant with culture filtrates of HBNR significantly increased before and
after inoculation of pathogens as compared to the control. Significant enhancement was
also observed in the fast-moving anodic peroxidase isozymes in the treated plants with
culture filtrates of HBNR. The results showed the elicitor(s) contained in culture filtrates
in HBNR. The lignin deposition as well as the peroxidase activity is an important step to
prevent systemically immunised plants from pathogen infection.
Keywords: Hypovirulent Binucleate Rhizoctonia (HBNR), Induced Systemic Resistance,
Colletotrichum orbiculare, Cucumber
*
Corresponding author: a_muslim@unsri.ac.id
© Penerbit Universiti Sains Malaysia, 2019. This work is licensed under the terms of the Creative
Commons Attribution (CC BY) (http://creativecommons.org/licenses/by/4.0/).A. Muslim et al.
INTRODUCTION
Induced resistance is the phenomenon in which a plant, once appropriately
stimulated, exhibits an enhanced resistance upon challenge inoculation with a
pathogen. It can be localised as well as systemic, and can be induced by limited
pathogen infection, virulent or avirulent pathogens, certain non-pathogenic
bacteria, cell wall fragments, plant extracts and certain chemicals (Van Loon 2000;
Walters 2010).
Concerns about impacts of agrichemicals on food safety and the
environment are related to the danger of the synthetic pesticide utilisation,
leading plant pathologists to develop another sustainable control for managing
plant disease (Hyakumachi et al. 2014). Elicitors of host resistance are a potential
alternative control to plant diseases (Lyon et al. 1995).
Several investigations have reported that cucumber anthracnose caused by
Colletotrichum orbiculare could be effectively control by endophytic Streptomyces
(Shimizu et al. 2009), Rhizobacteria, Bacillus pumilus, Bacillus subtilis and
Curtobacterium flaccumfaciens (Raupach & Kloepper 2000). Some studies show
induced systemic resistance in cucumbers against antrachnose using biotic and
abiotic elicitor. Meera et al. (1994) demonstrated that a sterile fungus and Phoma
sp. were reliable in activating the systemic resistance of cucumber against the
anthracnose disease. Koike et al. (2001) demonstrated that fungi isolated from
zoysiagrass (Zoysia tenuifolia) rhizosphere (Penicillium, Trichoderma, Phoma,
Fusarium, and a sterile fungus) significantly induced systemic resistance against
cucumber anthracnoses. This is done through lignification enhancement and
superoxide generation. Tian et al. (2008) reported that application of Pieris rapae
extract onto the first true cucumber leaves effectively brought about systemic
resistance against cucumber anthracnose with the enhancement of peroxidase
and polyphenoloxidase. Lin et al. (2014) demonstrated that protein lysis buffer
and a non-ionic detergent agent applied to separate cell membrane complexes
(Nonidet P-40) is effective to weaken cucumber anthracnose by triggering genes
related to disease resistance (peroxidase and pathogenis associated with protein
1-1a, acidic class III chitinase, phenylalanine ammonialyase 1). Research on
hypovirulent binucleate Rhizoctonia (HBNR) as a potential biocontrol agent
against Fusarium diseases in tomatoes and spinach have been recently reported
in our investigations with a mechanism that might be induced resistance (Muslim
et al. 2003a, 2003b, 2003c). There has also been an investigation of HBNR as an
agent of induced systemic resistance (ISR) on beans against Rhizoctonia solani or
C. lindermuthianum (Xue et al. 1998); they also protected cotton against alternaria
leaf spot and rhizoctonia damping-off with ISR (Jabaji-Hare & Neate 2005).
However, until now, there has been no report of the use of HBNR as an agent of
ISR on cucumber against anthracnose pathogen C. orbiculare (= C. lagenarium).
In general, ISR in plants is clearly defined as a set of induced defense
responses, including the creation of cell wall lytic enzymes. For example,
1,3-β-glucanases and chitinases (Lowton & Lamb 1987) enhance the activities
of peroxidase and lignin deposition, callose, hydroxyproline-rich glycoprotein
110Induction of Systemic Resistance in Cucumber
(Hammerschmidt & Kuc 1982; Hammerschmidt et al. 1982; Hammerschmidt et al.
1984); and phytoalexins (Ebel 1986).
Various agents both abiotic and biotic inducer (e.g., virulent or avirulent
pathogens, nonpathogen microorganisms, cell wall fragments, plant extracts, and
synthetic chemicals) have been documented to induce resistance after challenging
with pathogen attack, both locally and systemically (Walters et al. 2005). Plants
possess various inducible defense mechanisms to protect themselves against
pathogens. These defense mechanisms include preexisting physical and chemical
barriers, as well as inducible defense responses. The pre-existing biochemical
defense mechanisms include phenolics, phenolic glycosides, unsaturated
lactones, saponins, cyanogenic glycosides, glucosinolates, 5-alkylated resorcinols
and dienes (Osbourn 1996). The inducible defenses include the production of
reactive oxygen species (ROS), hypersensitive response, reinforcement of cell
wall, phytoalexins production and pathogenesis-related (PR) proteins (Mellersh &
Heath 2004).
This study aims to investigate HBNR capacity in inducing systemic
resistance in cucumber against C. orbiculare. The study was designed to reveal if
induced resistance in cucumber is correlated with enhanced systemic lignification
and peroxidase activity.
MATERIALS AND METHODS
Isolates
Hypovirulent binucleate Rhizoctonia isolate of W1, W7 (AG-A), L1 (AG-Ba), and
Rhv7 (unknown anastomosis group) obtained from soil samples were used as
biocontrol agents. The pathogens used in this study were Colletotrichum orbiculare
(Berk & Mont.) Arx (=Colletotrichum lagenarium (Pass.) Ellis & Halst.) isolate 104T,
which were obtained from infected cucumber plants.
Plants
Throughout the experiment, cucumber cv. Gibai was used. Before the sowing,
seeds were sterilised with 70% ethyl alcohol for one minute, and 1% of NaOCl for
20 min. Finally, they were rinsed in sterilised distilled water three times.
Inoculum Preparation
Isolates of pathogen C. orbiculare were cultured on potato dextrose agar (PDA)
as long as seven days without exposure to light. The temperature was maintained
at 25°C. A sterilised glass bar from the cultures with added sterile water, and
scraped the spore suspensions. The spore suspension was then filtered through
eight layers of sterile gauze. The isolates were set as two inoculum forms: barley
grain inoculum and culture filtrate.
111A. Muslim et al.
The following procedure was used for preparation of barley grain
inoculum: Each isolate was cultured in PDA for three days without light and at
room temperature. Five 5 mm mycelial disks of the culture were applied to 100 g of
moist autoclaved barley grains (1:1, w/v dry barley grains/distilled water) collected
in a 500 mL Erlenmeyer flask. The cultures were maintained and regularly shaken
for 10 days at 25°C to produce well-colonised inoculum with HBNR. The inoculum
was naturally dried for around 10 days. They were then kept refrigerated at 4°C
until use.
The following procedure was used for the culture filtrate (CF): Two mycelial
disks of each HBNR isolate obtained from the culture growing on PDA were put
into a 20 mL flask with 50 mL of potato dextrose broth (pH 6.5). The isolates
were grown in static conditions at 23°C–25°C for 10 days without light. The CF
separated from the mycelia. Next, the CF was filtered three times over three layers
of Whatman filter paper number 2. The CF was also filtered and sterilised using
millipore filtration (0.45 µm Millipore filters, Millipore Products Division, Bedford,
USA).
Cucumber ISR Assays
Experiments with barley grain inocula
Each sterilised plastic pot, sized ø 6 cm x 7.5 cm, was filled with the colonised
barley grain inocula mixture (2%, w/w) with as much as 120 g of potting medium.
The previously-sterilised (with 0.5% NaOCl) cucumber seeds were added to the
mixture. Each pot was given one seed. Next, the plants were cultivated at 25°C.
This required 21 days in a growth chamber with a 14 h light (24,000 lux) per dark
period. The plants that were grown in the potting medium with untreated barley
grain inocula were used as a control. Each inocula of HBNR isolate was inoculated
on six plants as replication and the experiment was repeated twice.
Experiment with culture filtrates (CF)
The plastic pots (autoclavable, ø6 cm x 7.5 cm) containing about 120 g of potting
medium were heated in autoclaves. The surface-sterilised cucumber seeds were
sown in each pot. The plants were maintained in a similar manner as previously
described. The first true leaves of 21-day-old cucumber plants were soaked with
CF for 1 min. The plants were inoculated after 24 h of incubation. Each CF of
HBNR isolate was applied on six plants as replication and the experiment was
repeated twice.
Challenge inoculation
The second true leaves were inoculated with 20 individual drops (each drop was
10 µl) of spore suspension of C. orbiculare (5 × 105 spores/mL). The disk of lens
112Induction of Systemic Resistance in Cucumber
paper (ø 5 mm) was covered on every drop toward the run-off prevention. This
was done to ensure the distribution of equal numbers of spores along the leaf
surfaces. The inoculated plants were maintained for 48 h without light at 25°C in a
humid chamber (85%–90% RH). After that, for six days the inoculated plants were
brought to the growth chamber. The total number per leaf and diameter of lesion
per inoculated drop were measured.
Testing for Lignin Formation
The cucumber seeds were grown on damp sterilised filter paper. Next, they
were incubated for a week without light at 25°C. The roots of the seedlings were
put in 5.0 mL of CF and incubated for one day. Then, with 10 µl drops of spore
suspension (5 × 105 spores/mL) of C. orbiculare, the hypocotyls of the treated
seedlings were inoculated. Next, the inoculated seedlings were incubated for 20 h.
The epidermal strips of the seedling hypocotyls were stained with toluidine blue O
or phloroglucinol-HCL (Sherwood & Vance 1976). They were observed under the
microscope to reveal percentage of lignification.
Spores of C. orbiculare germinated 90% or more on cucumber hypocotyls.
The degree of lignin deposition was evaluated by determining the percentage of
germinated spores together with appressoria around which lignin depositions were
induced. For each treatment 100 germinated spores were evaluated.
Protein Extraction and Determination
Treated cucumber root seedlings with CF of HBNR and challenge inoculated with
C. orbiculare were prepared as described previously in section of testing for lignin
formation. Samples were collected from seedlings prior to the time of challenge
inoculation and again 8–48 h after the challenge inoculation. All samples were
immediately frozen at –80°C until peroxidase assays were performed. Only the
hypocotyls of the cucumber seedlings were used for protein extraction. These
samples were homogenised in 5 mL of 0.05 M sodium phosphate buffer at pH
6.0 per 1 g sample with a cold mortar and pestle. The extract was centrifuged
at 10,000 rpm for 10 min at 4°C, and the supernatant was used to analyse the
peroxidase activity. To determine the protein contents of these extracts, the Lowry
method (Lowry et al. 1951) was used with bovine serum albumin as the standard.
Assay for Peroxidase Activity
Peroxidase activities were assessed following the method of Dalisay and Kuc
(1995). They were determined using guaiacol, which acted as the hydrogen donor.
The reaction mixture (3 mL) contained 0.25% (v/v) guaiacol in 1 mM sodium
phosphate buffer at pH 6.0 with 100 mM hydrogen peroxidase. In order to catalyse
the reaction, one-tenth ml crude enzyme extract was added and continued with
colorimetrically at 470 nm min−1 mg−1 protein.
113A. Muslim et al.
Detection of Peroxidase Isozymes by Gel Electrophoresis
Native PAGE was done with a PhastSystem (Pharmacia LKB, UK). Extracts were
adjusted to the same protein concentration with phosphate buffer and then loaded
onto an 8%–25% gradient gel. A peroxidase isoenzyme was made visible by
immersing the extracts in gels of 1% o-dianisidine solution. After 10 min, the gels
were cleaned with distilled water. They were then placed into 0.06% H2O2 solution
to concretely show the peroxidase isoenzyme bands.
Data Analysis
The experiments in this study were designed in completely randomised designs.
Total lesion numbers, anthracnose lesion diameters, and lignin formation in this
study were compared using Fisher’s least significant difference (LSD) test at
P = 0.05 and P = 0.01.
RESULTS
ISR in Cucumber Against Anthracnose with HBNR
This study showed that the use of barley grain inoculum and CF of HBNR isolates
significantly (P = 0.05) decreased total anthracnose lesion diameter compared to
the control (Table 1). However, no significant reduction was observed in total lesion
number (Table 1). The reduction of total lesion diameter by barley grain inoculum
of HBNR L2, W1, W7, and Rhv7 was 28%, 44%, 39% and 40%, respectively.
Similar results were also observed in the treatment with CF; the reduction of total
lesion diameter by CF of HBNR L2, W1, W7, and Rhv7 was 45%, 46%, 42%, and
48%, respectively (Table 1).
Lignin Formation and Peroxidase Activities in Cucumber Hypocotyls Treated
with HBNR
Lignin formation was observed as the intense blue and green colours of the
lignified cell walls. Cucumber hypocotyls pretreated with CF of HBNR L2, W1, W7,
and Rhv7 significantly increased lignin deposition in places that had been infected
by C. orbiculare compared to the control treatment (Fig. 1). Cucumber seedlings
treated with CF of HBNR L2, W1, W7, and Rhv7 increased lignin deposition by
1.45-fold, 1.71-fold, 1.04-fold, and 1.81-fold, respectively, relative to control.
114Induction of Systemic Resistance in Cucumber
Table 1: Effect of HBNR isolates on the total lesion number and lesion diameter on leaves
of cucumber plants that have been challenge inoculated with Colletotrichum orbiculare.
Total lesion numbera Total lesion diameter (mm)a
Treatments
BGIb CFc BGI CF
Pathogen 19.5 a
16.8 a
123.5 b
89.3 b
HBNR L2 16.8 a 12.5 a 89.5 a 48.7 a
HBNR W1 16.0 a 13.1 a 68.7 a 48.1 a
HBNR W7 17.2 a
12.9 a
75.5 a
51.8 a
HBNR Rhv7 16.8 a 11.7 a 74.5 a 46.5 a
Notes: a Mean of two trials each with six plants per treatment. Values followed by the same letter do not differ
significantly (P = 0.05) according to Fisher’s least significant difference test.
b
Plants were grown in potting medium amended with barley grain inoculum (BGI) of HBNR isolates (1%, w/w)
for 21 days and challenge inoculated with 10 µl drops of 5 x 105 spores/ml of C. orbiculare at 20 locations on the
second true leaves.
c
The first true leaves of 21-day-old cucumber plants grown in potting medium were treated with CF of HBNR and
challenge inoculated with C. orbiculare on the second true leaves as described above.
Figure 1: Lignification of hypocotyls of cucumber seedlings induced by culture filtrates of
HBNR, following challenge inoculation with Colletotrichum orbiculare. Cucumber seedlings
treated with sterilised distilled water were used as control. The hypocotyls of treated
plants were challenged with 5 µl drops of 105 spores/ml of C. orbiculare at 10 locations.
Bars labeled with the same letter are not significantly different according to Fisher’s least
significant difference test (P = 0.01).
Peroxidase activities in cucumber hypocotyls sampled at varying times
before and after challenge inoculation were higher in the plant treated with
HBNR compared to the control (Fig. 2). Treatment with HBNR L2, W1, W7 and
Rhv7 increased peroxidase activities by 40%, 70%, 57%, and 81%, respectively,
before inoculation of C. orbiculare, and by 39%–64%, 33%–94%, 43%–58%, and
23%–94%, respectively, relative to control after inoculation of C. orbiculare.
115A. Muslim et al.
Figure 2: Time course of peroxidase activity in hypocotyls of cucumber after treating the
root with HBNR isolates and challenge inoculating with C. orbiculare. Peroxidase activity is
expressed as changes in absorbance min−1 mg−1 protein. Cucumber seedlings treated with
sterilised distilled water were used as control. Data are the mean of three replications with
five seedlings (cucumber) per replication. Bars represent standard error of the mean. 0 h
indicates time before pathogen inoculation.
Figure 3: Electrophoresis patterns of peroxidase isozyme (POX 1 and POX 2) cucumber
seedlings treated with HBNR (Protein concentration was 0.1 mg/ml). Cucumber seedlings
treated with sterilised distilled water were used as control.
116Induction of Systemic Resistance in Cucumber
Two peroxidase isozymes (isoforms 1 and 2) were found in cucumber
hypocotyls. The fast-moving anodic peroxidase isozymes were enhanced gradually
after challenge inoculation. The peroxidase activities increased in the isoform 2 in
the seedlings treated with HBNR compared to the control, at all sampling times,
according to band intensity and width (Fig. 3). Isozyme type 1 had a minor activity
band and was observed after 48 h of pathogen inoculation either on inoculated or
non-inoculated with pathogen.
DISCUSSION
This study reveals that treatment with HBNR isolates suppresses disease
development of anthracnose in cucumber. The disease development suppression
seemingly resulted from plant’s ISR, as separated inoculation sites between
HBNR and C. orbiculare, where the root was employed with HBNR isolates, and
C. orbiculare was inoculated on the leaves, or the first true leaves were treated
with HBNR isolates and C. orbiculare was challenge inoculated on the second
true leaves. Thus, HBNR and pathogen application sites were separated spatially,
and no HBNR isolates could be recovered from the second true leaves. The result
of this research supports the evidence that the mechanism of protection from
R. solani by HBNR is induced resistance (Cardoso & Echandi 1987; Poromarto
et al. 1998).
A report presented by Xue et al. (1998) showed that inoculation of bean
hypocotyls with HBNR induced systemic resistance and protection of the roots
and cotyledon to later challenges not only with the root rot pathogen R. solani but
also with the anthracnose pathogen C. lindemuthianum. This study applied HBNR
as barley grain inoculum, and CF induced systemic resistance in cucumber plants
against C. orbiculare. Similar methods were used by Meera et al. (1994) and Koike
et al. (2001), in which plant-growth-promoting fungi (PGPF) were applied at the
root as barley grain inoculum, mycelia inoculum, or culture filtrates. This induced
systemic resistance in cucumber after being challenged with C. orbiculare in leaves.
Another study reported that germinating tomato seeds for one week in chemicals
of b-aminobutyric acid (BABA) and jasmonic acid (JA) solutions promoted seed
germination efficiency and induced resistance in four-week-old plants (Luna et al.
2016).
In this study, when HBNR CF was applied at the cucumber roots, lignin
was enhanced at the attempted penetration by the pathogen in the epidermal
tissues of cucumber hypocotyls. Enhanced lignin deposition was positively
correlated with significant reduce of lesion development. Lignin may improve
plant resistance against fungal infection through enhanced physical barrier and
chemical direct toxicity through their toxic derivatives such as phenolic compounds
(Xue & Yi 2017). Our results also show that peroxidase activity in hypocotyls in
the treated cucumber plant with HBNR significantly increased before and after
inoculation of the pathogen compared to the control. Significant enhancements
117A. Muslim et al.
were also observed in the fast-moving anodic peroxidase isozymes (isoform 2)
in the plants treated with HBNR. Isoform 1 may have less significant role in
induce resistance since it showed a minor activity and found on both inoculated
and non-inoculated hypocotyl. This supports the finding by Xue et al. (1998) that
inoculation of bean hypocotyls with HBNR induced systemic resistance, and this
was positively correlated with peroxidase. Arora and Bajaj (1985) and Krstic et al.
(1997) also reported that infection of mung bean and strawberry with binucleate
Rhizoctonia resulted in an increase in peroxidase activity. Peng et al. (2004) found
that pretreated cucumber seedlings with pectinase extract derived from Penicillium
oxalicum BZH-2002 fermentation products resulted in induced resistance toward
cucumber scab Cladosporium cucumerinum through the increased defense-
related enzymes, polyphenol oxidase, and peroxidase.
Increased peroxidase activity is also well observed in rhizobacteria-
induced systemic resistance. Chandrasekaran and Chun (2016) demonstrated
that treating tomato plants with Bacillus subtilis CBR05 significantly enhanced the
activities of antioxidant enzymes including peroxidase. Yanti (2015) reported that
rhizobacteria enhanced peroxidase enzyme activity. The isolate PK2Rp3 (Serratia
marcescens strain N2.4) showed the highest activity of both roots and leaves of
0.058 μg · mL–1 and 0.053 μg · mL–1.
According to Dean and Kuc (1987) and Hammerschmidt et al. (1984),
lignin deposition was considered a crucial phase of pathogen suppression in
systemically immunised plants. Vance et al. (1980) reported that rapid lignin
deposition might lead to the production of chemical or physical barriers to pathogen
infection. Furthermore, peroxidases accelerate the ending polymerization step of
lignin synthesis, resulting in the enhanced capability of protected tissue (Gross
1979). In the other studies, the enhanced peroxidase activities are often related to
resistance phenomenon such as the production of lignin (Hammerschmidt & Kuc
1982; Ride 1975). Peng and Kuc (1992) discovered the implications of peroxidase
towards oxidative defense mechanisms in treated plants with infections. The
peroxidase-generated hydrogen peroxidase directly functions as an antimicrobial
agent. In our study, when plant treated with barley grain inoculum and CF of HBNR
isolates, significant reduction was observed in total lesion diameter. However, no
significant reduction was observed in total lesion number. This result indicated
that increased lignification and peroxidase activities observed in this study did not
restrict total penetration of C. orbiculare. The data suggest that the involvement of
other defense mechanism(s) acting at the level of restricting lesion development to
fungal infection. Lignification and peroxidase activities, alone or collectively, are not
sole determinants for induced systemic resistance. Van Loon (2000) indicated that
induced resistance is the result of multi-mechanisms. Therefore, it is necessary to
investigate further other mechanisms, alone or collectively, involved in systemic
resistance against C. orbiculare. Further research is needed to identify other PR-
proteins that may be involved in the mechanism of cucumber ISR from HBNR.
118Induction of Systemic Resistance in Cucumber
The abilities of HBNR isolates to induce systemic resistance in cucumber
against anthracnose and to enhance lignin deposition and peroxidase activity as
well as their effectiveness against Fusarium diseases in tomato and spinach in our
previous studies (Muslim et al. 2003a, 2003b, 2003c), shows significant potential
as a bio-control agent to manage Colletotrichum orbiculare and other diseases.
CONCLUSION
Plant treated with barley grain inoculum and culture filtrate of HBNR isolates
effectively reduced lesion development of anthracnose in cucumber with induced
systemic resistance mechanism through enhancing lignin deposition and
peroxidase activity.
ACKNOWLEDGEMENTS
We thank the Ministry of Education, Science, Sports, and Culture (Monbukagakusho)
Japan, for financial assistance.
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